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Coexistence of Y, W, and Z Sex Chromosomes in Xenopus Tropicalis

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Coexistence of Y, W, and Z Sex Chromosomes in Xenopus Tropicalis Coexistence of Y, W, and Z sex chromosomes in PNAS PLUS Xenopus tropicalis Álvaro S. Rocoa, Allen W. Olmsteadb,1, Sigmund J. Degitzb, Tosikazu Amanoc, Lyle B. Zimmermanc, and Mónica Bullejosa,2 aDepartment of Experimental Biology, Faculty of Experimental Sciences, University of Jaén, Las Lagunillas Campus S/N, 23071 Jaén, Spain; bMid-Continent Ecology Division, Environmental Protection Agency, Duluth, MN 55804; and cDivision of Developmental Biology, Medical Research Council-National Institute for Medical Research, London, NW7 1AA, United Kingdom Edited by David C. Page, Whitehead Institute, Cambridge, MA, and approved July 1, 2015 (received for review March 28, 2015) Homomorphic sex chromosomes and rapid turnover of sex-determin- (3, 16, 17). Nevertheless, not all sex chromosomes are morpho- ing genes can complicate establishing the sex chromosome system logically distinct. This lack of differentiation does not always in- operating in a given species. This difficulty exists in Xenopus tro- dicate a recent origin of the sex chromosomes, as is the case in picalis, an anuran quickly becoming a relevant model for genetic, ge- ratite birds and boid snakes (18, 19). Two hypotheses have been nomic, biochemical, and ecotoxicological research. Despite the recent proposed to explain the lack of differentiation between some pairs interest attracted by this species, little is known about its sex chromo- of sex chromosomes: (i) occasional recombination between them, some system. Direct evidence that females are the heterogametic sex, as could happen in sex-reversed individuals (20), and (ii)frequent as in the related species Xenopus laevis, has yet to be presented. turnover of sex chromosomes because of rapid changes of sex- Furthermore, X. laevis’ sex-determining gene, DM-W, does not exist determining genes, preventing sex chromosome differentiation (21). in X. tropicalis, and the sex chromosomes in the two species are not Amphibians present genetic sex determination (GSD), with X. tropicalis’ homologous. Here we identify sex chromosome system temperature affecting sex differentiation in some species of the i ii by integrating data from ( ) breeding sex-reversed individuals, ( )gy- genera Pleurodeles, Hynobius, Bufo, and Rana and artificial iii iv nogenesis, ( ) triploids, and ( ) crosses among several strains. Our polyploids of the genus Xenopus (11, 22, 23). Despite ubiquitous results indicate that at least three different types of sex chromosomes GSD, the sex chromosome pair has been identified in only about exist: Y, W, and Z, observed in YZ, YW, and ZZ males and in ZW and 4% of analyzed species (24), not because of the lack of cyto- GENETICS WW females. Because some combinations of parental sex chromo- logical studies [more than 25% of known Anura taxa have been somes produce unisex offspring and other distorted sex ratios, under- karyotyped (25, 26)], but because amphibian sex chromosomes standing the sex-determination systems in X. tropicalis is critical for developing this flexible animal model for genetics and ecotoxicology. are usually homomorphic (25). The diploid pipid frog Xenopus tropicalis has become an impor- tant model for developmental biology, genetics, evolutionary sex chromosomes | sex determination | sex reversal | gynogenesis | Xenopus tropicalis genomics, and ecotoxicology, but little is known about its sex chromosome system or mechanism of sex determination. All spe- cies from the genus Xenopus have homomorphic sex chromosomes ex chromosomes are unique karyotype features present only (27), including Xenopus laevis (28). However, breeding sex-reversed in species with genetic sex determination. They originate S animals shows that females are the heterogametic sex in X. laevis from autosomes when a gene/locus assumes the sex-determining (29–31). Thus, estradiol treatment during development results in role either by acquisition of a sex-specific trigger or by gene dosage effects on gonadal differentiation (1). Two main sex sex-reversed genetically male, phenotypically female animals, which chromosome systems can be found in vertebrates with genetic produce all-male offspring when mated to normal untreated males. sex determination: XX/XY (in which males are heterogametic) Conversely, sex-reversed females obtained by exposure to grafts of and ZZ/ZW (with heterogametic females). Nevertheless, sex testicular tissue produce offspring with a female:male sex ratio of chromosomes are extraordinarily variable, and other combina- tions also can be found, ranging from female heterogamety with Significance 00/0W or ZZ/Z0 sex chromosomes (2, 3) to male heterogamety with XX/X0 sex chromosomes (3). Furthermore, complex XY As in most amphibians, sex chromosomes of the model species and ZW systems are possible when fusions, fissions, and trans- Xenopus tropicalis are homomorphic, complicating identification locations between sex chromosomes and autosomes take place of the heterogametic sex. Using genetic approaches, we have (e.g., X1X2Y, XY1Y2,orZ1Z2W) (for a review see ref. 1). proved the existence of three types of sex chromosomes (Y, W, Among vertebrates, amphibians, reptiles, and fish show remark- and Z), defining three kinds of males (YZ, YW, and ZZ) and two able variation in sex-determining mechanisms and sex chromosome kinds of females (ZW and WW). The existence of both male and systems, not only between closely related species but even within female heterogametic individuals in one species is an extremely species. Taxa have been described with environmental sex determi- rare situation in nature, because some sex chromosome combi- nation and cryptic sex chromosomes in reptiles (4), multiple sex nations produce offspring with sex ratios different from 1:1. Thus, chromosomes and polyfactorial sex determination in amphibians and parental sex chromosomes must be taken into account when X tropicalis fishes (5–7), and frequent transitions between ZZ/ZW and XX/XY . is used in multigeneration genetic studies or in eco- sex chromosome systems in related species (8–11), with the extreme toxicological assays of endocrine disruptors with gender effects. example of Rana rugosa, in which both sex chromosome systems are Author contributions: Á.S.R., A.W.O., S.J.D., L.B.Z., and M.B. designed research; Á.S.R., differentiating independently in different populations (12). A.W.O., T.A., L.B.Z., and M.B. performed research; Á.S.R., A.W.O., S.J.D., L.B.Z., and M.B. It has been proposed that sex chromosomes differentiate when a analyzed data; and Á.S.R., L.B.Z., and M.B. wrote the paper. sex-determining region accumulates sexually antagonistic alleles, The authors declare no conflict of interest. favoring suppression of recombination (13). Nonrecombining regions This article is a PNAS Direct Submission. of sex-specific chromosomes (Y and W) degenerate progressively, 1Present address: Bayer CropScience, Research Triangle Park, NC 27709. leading eventually to cytogenetically distinct heteromorphic sex 2To whom correspondence should be addressed. Email: [email protected]. chromosomes (14, 15). In the most extreme cases, the Y or W This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. chromosome is lost entirely, resulting in the X0 and Z0 systems 1073/pnas.1505291112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1505291112 PNAS Early Edition | 1of10 Downloaded by guest on September 25, 2021 3:1 (30). Among the female offspring from these sex-reversed fe- Table 1. Sex ratios observed in clutches after different males, one third were predicted to be WW “superfemales,” confirmed treatments with synthetic estrogens by crosses to normal males resulting in all-female clutches (31). Strain Estrogen Dose, μg/L No. females No. males The only sex-determining gene identified in amphibians to date is the DM-W gene from X. laevis (32). This gene is located golden EE2 0.640 24* 0 † on the W chromosome of this species (32, 33), confirming the (N/ICF1)IC β-Estradiol 10 40 2 female heterogamety previously demonstrated by sex-reversal (N/ICF1)IC β-Estradiol 50 14‡ 0 experiments. However, DM-W is present in only some Xenopus Total 78 2 species and not in X. tropicalis or other amphibians (34). EE2, ethynylestradiol. Genetic markers linked to the X. tropicalis sex-determining *Females identified in three spawns (n = 8 each). † locus were identified in an amplified fragment-length polymor- All males with small testes. ‡ phism study (35). These markers largely place to sequence scaf- Some females were sterile. folds that genetically map to the short arm of linkage group 7 (chromosome 7) (36, 37). Although it has been proposed that X. tropicalis’ sex chromo- (i.e., WW) were mated with control males. Consistent with a some system is similar to that of X. laevis (33, 35, 36), experimental maternal WW genotype, the offspring were all female, indicating support for this hypothesis is limited. Here we provide the first that these matings were ♀ WW × ♂ ZZ = ♀ ZW. For a pedigree (to our knowledge) description of the sex chromosome system of of the sex-reversal experiment, see Figs. S1 and S2. X. tropicalis, integrating data from (i) breeding sex-reversed in- dividuals, (ii) gynogenesis (both gynogenetic diploids and com- Sex of Gynogenenetic Offspring. Production of viable diploid ani- pletely homozygous double haploids), (iii) triploids, and (iv) crosses mals derived solely from the maternal genome, or gynogenesis, among several laboratory strains. Our analysis shows that both provides an independent method for analyzing sex-determination males and females in X. tropicalis can be either homogametic or systems. Two different methods can be used to rescue viable dip- heterogametic. At least three different types of sex chromosomes loid embryos from nonviable haploids (produced by fertilization exist: Y, W, and Z, observed in YZ, YW, and ZZ males and ZW with UV-irradiated sperm) (Fig. 2A): (i) suppressing polar body and WW females. Because some parental combinations can lead to extrusion by early cold shock (ECS), and (ii) suppressing first unisex offspring or other distorted sex ratios, understanding the sex cleavage following DNA replication by late cold shock (LCS). determination systems in X.
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